Opposing muscarinic and nicotinic modulation of hypoglossal motor output to genioglossus muscle in rats in vivo

Journal of Physiology

Volumn 565, Issue 3, 2005, Pages 965-980

  Liu, Xia ^a   Sood, Sandeep ^a   Liu, Hattie ^a   Horner, Richard L ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1,1 DIMETHYL 4 PHENYLPIPERAZINIUM; 1,1 DIMETHYL 4 PHENYLPIPERAZINIUM IODIDE; ACETYLCHOLINE; ATROPINE; CARBACHOL; DIHYDRO BETA ERYTHROIDINE; MUSCARINE; MUSCARINIC RECEPTOR; NICOTINIC RECEPTOR; PHYSOSTIGMINE; URETHAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING; CHOLINERGIC STIMULATION; CONTROLLED STUDY; GENE ACTIVATION; GENIOGLOSSUS MUSCLE; HYPOGLOSSAL NUCLEUS; IN VIVO STUDY; MALE; MICRODIALYSIS; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SLEEP APNEA SYNDROME; TONGUE; ADULT; EXCITABILITY; HYPOGLOSSAL MOTOR NUCLEUS; MUSCLE CONTRACTION;

ANIMALS; ATROPINE; CARBACHOL; CARBON DIOXIDE; CHOLINERGIC AGONISTS; DIMETHYLPHENYLPIPERAZINIUM IODIDE; HYPOGLOSSAL NERVE; MALE; MECAMYLAMINE; MICRODIALYSIS; MOTOR NEURONS; MUSCARINIC ANTAGONISTS; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC; TONGUE;

EID: 21344472381     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.084657     Document Type: Article

References (59)

1. Alessandri B, Landolt H, Langemann H, Gregorin J, Hall J & Gratzl O (1996). Application of glutamate in the cortex of rats: a microdialysis study. Acta Neurochirurgica - Suppl 67, 6-2.
2. 2 on upper airway and respiratory pump muscle activity in the rat. J Physiol 532, 525-534.
3. Bellingham MC & Berger AJ (1996). Presynaptic depression of excitatory synaptic inputs to rat hypoglossal motoneurons by muscarinic M2 receptors. J Neurophysiol 76, 3758-3770.
4. Bellingham MC & Funk GD (2000). Cholinergic modulation of respiratory brain-stem neurons and its function in sleep-wake state determination. Clin Exp Pharmacol Physiol 27, 132-137.
5. Chamberlin NL, Bocchiaro CM, Greene RW & Feldman JL (2002). Nicotinic excitation of rat hypoglossal motoneurons. Neuroscience 115, 861-870.
6. Connaughton M, Priestley JV, Softoniew MV, Eckenstein F & Cuello AC (1986). Inputs to motoneurones in the hypoglossal nucleus of the rat: light and electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17, 205-224.
7. Davidoff MS & Irintchev AP (1986). Acetylcholinesterase activity and type C synapses in the hypoglossal, facial and spinal-cord motor nuclei of rats. An electron-microscope study. Histochemistry 84, 515-524.
8. Dobbins EG & Feldman JL (1995). Differential innervation of protruder and retractor muscles of the tongue in rat. J Comparative Neurol 357, 376-394.
9. el Mansari M, Sakai K & Jouvet M (1989). Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76, 519-529.
10. Fogel RB, White DP, Pierce RJ, Malhotra A, Edwards JK, Dunai J, Kleverlaan D & Trinder J (2003). Control of upper airway muscle activity in younger versus older men during sleep onset. J Physiol 553, 533-544.
11. Fuller DD, Williams JS, Janssen PL & Fregosi RF (1999). Effect of co-activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat. J Physiol 519, 601-613.
12. Funk GD, Smith JC & Feldman JL (1993). Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70, 1497-1515.
13. Gothe B, Strohl KP, Levin S & Cherniack NS (1985). Nicotine: a different approach to treatment of obstructive sleep apnea. Chest 87, 11-17.
14. Greer JJ, Smith JC & Feldman JL (1991). Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437, 727-749.
15. Hamrahi H, Chan B & Horner RL (2001). On-line detection of sleep-wake states and application to produce intermittent hypoxia only in sleep in rats. J Appl Physiol 90, 2130-2140.
16. Haxhiu MA, Mitra J, van Lunteren E, Bruce EN & Cherniack NS (1984a). Hypoglossal and phrenic responses to cholinergic agents applied to ventral medullary surface. Am J Physiol 247, R939-R944.
17. Haxhiu MA, Van Lunteren E, Van de Graaff WB, Strohl KP, Bruce EN, Mitra J & Cherniack NS (1984b). Action of nicotine on the respiratory activity of the diaphragm and genioglossus muscles and the nerves that innervate them. Respir Physiol 57, 153-169.
18. Hedner J, Kraiczi H, Peker Y & Murphy P (2003). Reduction of sleep -disordered breathing after physostigmine. Am J Respir Crit Care Med 168, 1246-1251.
19. Hellstrom J, Oliveira AL, Meister B & Cullheim S (2003). Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J Comp Neurol 460, 476-486.
20. 2 in rats. J Appl Physiol 92, 878-887.
21. Jelev A, Sood S, Liu H, Nolan P & Horner RL (2001). Microdialysis perfusion of 5-HT into hypoglossal motor nucleus differentially modulates genioglossus activity across natural sleep-wake states in rats. J Physiol 532, 467-481.
22. Keifer JC, Baghdoyan HA, Becker L & Lydic R (1994). Halothane decreases pontine acetylcholine release and increases EEG spindles. Neuroreport 5, 577-580.
23. Keifer JC, Baghdoyan HA & Lydic R (1996). Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia. Anesthesiology 84, 945-954.
24. Kubin L & Fenik V (2004). Pontine cholinergic mechanisms and their impact on respiratory regulation. Respir Physiol Neurobiol 143, 235-249.
25. Kubin L, Tojima H, Davies RO & Pack AI (1992). Serotonergic excitatory drive to hypoglossal motoneurons in the decerebrate cat. Neuroscience Lett 139, 243-248.
26. Lape R & Nistri A (2000). Current and voltage clamp studies of the spike medium afterhyperpolarization of hypoglossal motoneurons in a rat brain stem slice preparation. J Neurophysiol 83, 2987-2995.
27. Lee LH, Friedman DB & Lydic R (1995). Respiratory nuclei share synaptic connectivity with pontine reticular regions regulating REM sleep. Am J Physiol 268, L251-L262.
28. Li M, Yasuda RP, Wall SJ, Wellstein A & Wolfe BB (1991). Distribution of m2 muscarinic receptors in rat brain using antisera selective for m2 receptors. Mol Pharmacol 40, 28-35.
29. Liu X, Sood S, Liu H, Nolan P, Morrison JL & Horner RL (2003). Suppression of genioglossus muscle tone and activity during reflex hypercapnic stimulation by GABA-A mechanisms at the hypoglossal motor nucleus in-vivo. Neuroscience 116, 249-259.
30. Lydic R & Baghdoyan HA (1993). Pedunculopontine stimulation alters respiration and increases ACh release in the pontine reticular formation. Am J Physiol 264, R544-R554.
31. Lydic R & Baghdoyan HA (2003). Neurochemical evidence for the cholinergic modulation of sleep and breathing. In Sleep-Related Breathing Disorders: Experimental Models and Therapeutic Potential, ed. Carley DW & Radulovacki M, pp. 57-91. Dekker, New York.
32. Lydic R, Baghdoyan HA, Wertz R & White DP (1991). Cholinergic reticular mechanisms influence state-dependent ventilatory response to hypercapnia. Am J Physiol 261, R738-R746.
33. Mallios VJ, Lydic R & Baghdoyan HA (1995). Muscarinic receptor subtypes are differentially distributed across brain stem respiratory nuclei. Am J Physiol 268, L941-L949.
34. 2 responses and the additive effects of GABA. J Appl Physiol 93, 1786-1796.
35. A receptor antagonism at the hypoglossal motor nucleus increases genioglossus muscle activity in NREM but not REM sleep. J Physiol 548, 569-583.
36. Morrison JL, Sood S, Liu H, Park E, Nolan P & Horner RL (2003b). Role of inhibitory amino acids in control of hypoglossal motor outflow to genioglossus muscle in naturally sleeping rats. J Physiol 552, 975-991.
37. 2, brainstem chemoreceptors and breathing. Prog Neurobiol 59, 299-331.
38. Nattie EE & Li AH (1990). Ventral medulla sites of muscarinic receptor subtypes involved in cardiorespiratory control. J Appl Physiol 69, 33-41.
39. Ochiai R, Guthrie RD & Motoyama EK (1989). Effects of varying concentrations of halothane on the activity of the genioglossus, intercostals, and diaphragm in cats: an electromyographic study. Anesthesiology 70, 812-816.
40. Paxinos G & Watson C (1998). The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
41. Rekling JC, Funk GD, Bayliss DA, Dong XW & Feldman JL (2000). Synaptic control of motoneuronal excitability. Physiol Rev 80, 767-852.
42. Remmers JE, deGroot WJ, Sauerland EK & Anch AM (1978). Pathogenesis of upper airway occlusion during sleep. J Appl Physiol Respiratory Environ Exercise Physiol 44, 931-938.
43. Robinson DM, Peebles KC, Kwok H, Adams BM, Clarke LL, Woollard GA & Funk GD (2002). Prenatal nicotine exposure increases apnoea and reduces nicotinic potentiation of hypoglossal inspiratory output in mice. J Physiol 538, 957-973.
44. Sauerland EK, Orr WC & Hairston LE (1981). EMG patterns of oropharyngeal muscles during respiration in wakefulness and sleep. Electromyogr Clin Neurophysiol 21, 307-316.
45. Shao XM & Feldman JL (2000). Acetylcholine modulates respiratory pattern: effects mediated by M3-like receptors in preBotzinger complex inspiratory neurons. J Neurophysiol 83, 1243-1252.
46. Shao XM & Feldman JL (2001). Mechanisms underlying regulation of respiratory pattern by nicotine in preBotzinger complex. J Neurophysiol 85, 2461-2467.
47. Sood S, Liu X, Liu H, Nolan P & Horner RL (2003). 5-HT at hypoglossal motor nucleus and respiratory control of genioglossus muscle in anesthetized rats. Respiratory Physiol Neurobiol 138, 205-221.
48. Steriade M, Datta S, Pare D, Oakson G & Curro Dossi RC (1990a). Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10, 2541-2559.
49. Steriade M, Pare D, Datta S, Oakson G & Curro Dossi R (1990 b). Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J Neurosci 10, 2560-2579.
50. Thakkar MM, Strecker RE & McCarley RW (1998). Behavioral state control through differential serotonergic inhibition in the mesopontine cholinergic nuclei: a simultaneous unit recording and microdialysis study. J Neurosci 18, 5490-5497.
51. Tsukamoto K, Yin M & Sved AF (1994). Effect of atropine injected into the nucleus tractus solitarius on the regulation of blood pressure. Brain Res 648, 9-15.
52. Vertes RP (1979). Brain stem gigantocellular neurons: patterns of activity during behavior and sleep in the freely moving rat. J Neurophysiol 42, 214-228.
53. Wamsley JK, Lewis MS, Young WS III & Kuhar MJ (1981). Autoradiographic localization of muscarinic cholinergic receptors in rat brainstem. J Neurosci 1, 176-191.
54. Wiegand L, Zwillich CW, Wiegand D & White DP (1991). Changes in upper airway muscle activation and ventilation during phasic REM sleep in normal men. J Appl Physiol 71, 488-497.
55. Woolf NJ (1991). Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37, 475-524.
56. Woolf NJ & Butcher LL (1989). Cholinergic systems in the rat brain. IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 23, 519-540.
57. Worsnop C, Kay A, Pierce R, Kim Y & Trinder J (1998). Activity of respiratory pump and upper airway muscles during sleep onset. J Appl Physiol 85, 908-920.
58. Young T, Palta M, Dempsey J, Skatrud J, Weber S & Badr S (1993). The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 328, 1230-1235.
59. Zaninetti M, Tribollet E, Bertrand D & Raggenbass M (1999). Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat. Eur J Neurosci 11, 2737-2748.